Joint associations of blood plasma proteins with overwinter survival of a large mammal

In many wild animal populations, hosts are at risk of parasites and malnutrition and resource costs of defence may be difficult to afford. We postulate that proteins, important in homeostasis and immunity, play a complex but central role in condition dependence and resource costs of mammalian immune defence. To test this, we measured plasma concentrations of albumin, total proteins. Self‐reactive antibodies and parasite‐specific IgG in female Soay sheep. Using a principal component analysis, we found a new metric of condition reflecting individual variation in acquisition, assimilation and/or recycling of plasma proteins that predicted overwinter survival. Controlling for this metric, an age‐dependent trade‐off between antibody titres and protein reserves emerged, indicating costs of mounting an antibody response: younger individuals survived best when prioritising immunity while older individuals fared better when maintaining high‐protein nutritional plane. These findings suggest fascinating roles for protein acquisition and allocation in influencing survival in wild animal populations.     

Survival costs of reproduction are mediated by parasite infection in wild Soay sheep

A trade‐off between current and future fitness potentially explains variation in life‐history strategies. A proposed mechanism behind this is parasite‐mediated reproductive costs: individuals that allocate more resources to reproduction have fewer to allocate to defence against parasites, reducing future fitness. We examined how reproduction influenced faecal egg counts (FEC) of strongyle nematodes using data collected between 1989 and 2008 from a wild population of Soay sheep in the St. Kilda archipelago, Scotland (741 individuals). Increased reproduction was associated with increased FEC during the lambing season: females that gave birth, and particularly those that weaned a lamb, had higher FEC than females that failed to reproduce. Structural equation modelling revealed future reproductive costs: a positive effect of reproduction on spring FEC and a negative effect on summer body weight were negatively associated with overwinter survival. Overall, we provide evidence that parasite resistance and body weight are important mediators of survival costs of reproduction.     

Experimental demonstration of a parasite‐induced immune response in wild birds: Darwin's finches and introduced nest flies

Ecological immunology aims to explain variation among hosts in the strength and efficacy of immunological defenses. However, a shortcoming has been the failure to link host immune responses to actual parasites under natural conditions. Here, we present one of the first experimental demonstrations of a parasite‐induced immune response in a wild bird population. The recently introduced ectoparasitic nest fly Philornis downsi severely impacts the fitness of Darwin's finches and other land birds in the Galápagos Islands. An earlier study showed that female medium ground finches (Geospiza fortis) had P. downsi‐binding antibodies correlating with presumed variation in fly exposure over time. In the current study, we experimentally manipulated fly abundance to test whether the fly does, in fact, cause changes in antibody levels. We manipulated P. downsi abundance in nests and quantified P. downsi‐binding antibody levels of medium ground finch mothers, fathers, and nestlings. We also quantified host behaviors, such as preening, which can integrate with antibody‐mediated defenses against ectoparasites. Philornis downsi‐binding antibody levels were significantly higher among mothers at parasitized nests, compared to mothers at (fumigated) nonparasitized nests. Mothers with higher antibody levels tended to have fewer parasites in their nests, suggesting that antibodies play a role in defense against parasites. Mothers showed no behavioral changes that would enhance the effectiveness of the immune response. Neither adult males, nor nestlings, had P. downsi‐induced immunological or behavioral responses that would enhance defense against flies. None of the parasitized nests fledged any offspring, despite the immune response by mothers. Thus, this study shows that, while the immune response of mothers appeared to be defensive, it was not sufficient to rescue current reproductive fitness. This study further shows the importance of testing the fitness consequences of immune defenses, rather than assuming that such responses increase host fitness.     

A further cost for the sicker sex? Evidence for male‐biased parasite‐induced vulnerability to predation

Males are typically the sicker sex. Data from multiple taxa indicate that they are more likely to be infected with parasites, and are less “tolerant,” or less able to mitigate the fitness costs of a given infection, than females. One cost of infection for many animals is an increased probability of being captured by a predator. A clear, hitherto untested, prediction is therefore that this parasite‐induced vulnerability to predation is more pronounced among males than females. We tested this prediction in the sexually size dimorphic guppy, Poecilia reticulata, in which females are typically larger than males. We either sham or experimentally infected guppies with Gyrodactylus turnbulli, elicited their escape response using an established protocol and measured the distance they covered during 60 ms. To discriminate between the effects of body size and those of other inherent sex differences, we size‐matched fish across treatment groups. Infection with G. turnbulli reduced the distance covered during the escape response of small adults by 20.1%, whereas that of large fish was unaffected. This result implies that parasite‐induced vulnerability to predation is male‐biased in the wild: although there was no difference in escape response between our experimentally size‐matched groups of males and females, males are significantly smaller across natural guppy populations. These results are consistent with Bateman's principle for immunity: Natural selection for larger body sizes and longevity in females seems to have resulted in the evolution of increased infection tolerance. We discuss the potential implications of sex‐ and size‐biased parasite‐induced vulnerability to predation for the evolutionary ecology of this host–parasite interaction in natural communities.     

Sex and hatching order modulate the association between MHC‐II diversity and fitness in early‐life stages of a wild seabird

Genes of the major histocompatibility complex (MHC) play a pivotal role in parasite resistance, and their allelic diversity has been associated with fitness variations in several taxa. However, studies report inconsistencies in the direction of this association, with either positive, quadratic or no association being described. These discrepancies may arise because the fitness costs and benefits of MHC diversity differ among individuals depending on their exposure and immune responses to parasites. Here, we investigated in black‐legged kittiwake (Rissa tridactyla) chicks whether associations between MHC class‐II diversity and fitness vary with sex and hatching order. MHC‐II diversity was positively associated with growth and tick clearance in female chicks, but not in male chicks. Our data also revealed a positive association between MHC‐II diversity and survival in second‐hatched female chicks (two eggs being the typical clutch size). These findings may result from condition‐dependent parasite infections differentially impacting sexes in relation to hatching order. We thus suggest that it may be important to account for individual heterogeneities in traits that potentially exert selective pressures on MHC diversity in order to properly predict MHC–fitness associations.     

Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies,health and survival

Despite our rapidly advancing mechanistic understanding of vertebrate immunity under controlled laboratory conditions, the links between immunity, infection and fitness under natural conditions remain poorly understood. Antibodies are central to acquired immune responses, and antibody levels circulating in vivo reflect a composite of constitutive and induced functional variants of diverse specificities (e.g. binding antigens from prevalent parasites, self tissues or novel non-self sources). Here, we measured plasma concentrations of 11 different antibody types in adult females from an unmanaged population of Soay sheep on St Kilda. Correlations among antibody measures were generally positive but weak, and eight of the measures independently predicted body mass, strongyle parasite egg count or survival over the subsequent winter. These independent and, in some cases, antagonistic relationships point to important multivariate immunological heterogeneities affecting organismal health and fitness in natural systems. Notably, we identified a strong positive association between anti-nematode immunoglobulin (Ig) G antibodies in summer and subsequent over-winter survival, providing rare evidence for a fitness benefit of helminth-specific immunity under natural conditions. Our results highlight both the evolutionary and ecological importance and the complex nature of the immune phenotype in the wild.     

Age-related variation in immunity in a wild mammal population

Age‐related changes in immunity are well documented in humans and laboratory mammals. Using blood samples collected from wild Soay sheep, we show that pronounced differences in T‐cell subsets and inflammatory markers amongst age classes are also evident under natural conditions. These shifts parallel those observed in mammals experiencing protected environments. We found progressive declines in the proportion of naïve CD4 T cells with age, a precipitous drop in γδ T cells after the second year of life and an increase in acute phase protein levels amongst geriatric sheep. Our findings suggest immune aging patterns observed in laboratory and domestic mammals may generalize to more complex, challenging environments and could have fitness costs under natural conditions.     

Not going with the flow: Locomotor activity does not constrain immunity in a wild fish

Immunity is a central component of fitness in wild animals, but its determinants are poorly understood. In particular, the importance of locomotory activity as a constraint on immunity is unresolved. Using a piscine model (Gasterosteus aculeatus), we combined a 25‐month observational time series for a wild lotic habitat with an open flume experiment to determine the influence of locomotor activity (countercurrent swimming) on natural variation in immune function. To maximize the detectability of effects in our flume experiment, we set flow velocity and duration (10 cm/s for 48 hr) just below the point at which exhaustion would ensue. Following this treatment, we measured expression in a set of immune‐associated genes and infectious disease resistance through a standard challenge with an ecologically relevant monogenean infection (Gyrodactylus gasterostei). In the wild, there was a strong association of water flow with the expression of immune‐associated genes, but this association became modest and more complex when adjusted for thermal effects. Our flume experiment, although statistically well‐powered and based on a scenario near the limits of swimming performance in stickleback, detected no countercurrent swimming effect on immune‐associated gene expression or infection resistance. The field association between flow rate and immune expression could thus be due to an indirect effect, and we tentatively advance hypotheses to explain this. This study clarifies the drivers of immune investment in wild vertebrates; although locomotor activity, within the normal natural range, may not directly influence immunocompetence, it may still correlate with other variables that do.     

Possible Influence of B Chromosomes on Genes Included in Immune Response and Parasite Burden in Apodemus flavicollis

Genetic background underlying wild populations immune response to different parasites is still not well understood. We studied immune response to multiple infections and to competition between different parasite species at different developmental stages in population of yellow-necked mouse, Apodemus flavicollis. Quantitative real-time PCR was used to investigate associations of MHC II-DRB, IL-10 and Tgf-β genes expressions with presence of intestinal parasites at different developmental stages. Furthermore, we were interested whether the host related characteristics (sex, age, body condition, presence of B chromosomes or expression of other genes) or characteristics of present parasites (number of adult parasites of each identified species, egg count of each parasite genus, total number of nematode individuals) affect differential expression of the studied genes. A significant invert association between the expression of MHC II-DRB and Tgf-β gene was found, which together with absence of IL-10 association confirmed modified Th2 as the main type of immune response to nematode infections. Effect of recorded parasites and parasite life-cycle stage on expression levels of MHC II-DRB gene was detected only through interactions with host-related characteristics such as sex, age, and the presence of B chromosomes. The presence of B chromosomes is associated with lower expression level of Tgf-β gene. Although the influence of host genetic background on parasite infection has already been well documented, this is the first study in mammals that gave presence of B chromosomes on immune response full consideration.     

Weak relationships of parasite infection with sexual and life‐history traits in wild‐caught Texas field crickets (Gryllus texensis)

1. Sex differences in immune investment and infection rate are predicted due to the divergent life histories of males and females, where females invest more toward immunity due to the fitness consequences of a reduced lifespan and males allocate less toward immunity due to increased resource investment in traits critical to sexual selection. Consequently, males are expected to fight infection less adeptly, resulting in higher parasite loads relative to females across all taxa.
2. Wild animals rarely face a single parasite within their given environment, yet nearly all studies on sex‐biased infection rates have focused on a single host–parasite relationship. Here, we investigate how simultaneous natural infections of ecto‐ and endosymbionts (i.e. both parasitic and phoretic taxa) correlate with sex biases in host immune response and reproductive investment in a field‐caught cricket, Gryllus texensis.
3. Our comprehensive analysis found no significant sex differences in two measures of immune response (melanization and nodulation), and found no strong evidence of a sex bias in the prevalence or intensity of parasitism by the three most common parasites infecting wild G. texensis field crickets (Eutrombidiidae, gregarines, and nematodes).
4. Two traits related to female fitness, egg number and egg size, showed no relation to parasitic infection; however, males having wider heads and poorer body condition were significantly more infected by eutrombidiid mites, gregarines, and nematodes.
5. Despite frequent predictions of male‐biased parasitism in the literature, our results concur with many other studies indicating that the divergent life histories of males and females alone are not sufficient to explain natural infection rates in wild insects.

     

Generalist nematodes dominate the nemabiome of roe deer in sympatry with sheep at a regional level

The growth of livestock farming and the recent expansion of wild ungulate populations in Europe favor opportunities for direct and/or indirect cross-transmission of pathogens. Comparatively few studies have investigated the epidemiology of gastro-intestinal nematode parasites, an ubiquitous and important community of parasites of ungulates, at the wildlife/livestock interface. In this study, we aimed to assess the influence of livestock proximity on the gastrointestinal nematode community of roe deer in a rural landscape located in southern France. Using ITS-2 rDNA nemabiome metabarcoding on fecal larvae, we analysed the gastrointestinal nematode communities of roe deer and sheep. In addition, we investigated Haemonchus contortus nad4 mtDNA diversity to specifically test parasite circulation among domestic and wild host populations. The dominant gastrointestinal nematode species found in both the roe deer and sheep were generalist species commonly found in small ruminant livestock (e.g. H. contortus), whereas the more specialised wild cervid nematode species (e.g. Ostertagia leptospicularis) were only present at low frequencies. This is in marked contrast with previous studies that found the nemabiomes of wild cervid populations to be dominated by cervid specialist nematode species. In addition, the lack of genetic structure of the nad4 mtDNA of H. contortus populations between host species suggests circulation of gastrointestinal nematodes between roe deer and sheep. The risk of contact with livestock only has a small influence on the nemabiome of roe deer, suggesting the parasite population of roe deer has been displaced by generalist livestock parasites due to many decades of sheep farming, not only for deer grazing close to pastures, but also at a larger regional scale. We also observed some seasonal variation in the nemabiome composition of roe deer. Overall, our results demonstrate significant exchange of gastrointestinal nematodes between domestic and wild ungulates, with generalist species spilling over from domestic ungulates dominating wild cervid parasite communities.     

Fecal antibody levels as a noninvasive method for measuring immunity to gastrointestinal nematodes in ecological studies

Among‐individual variation in antibody‐associated immunity to gastrointestinal nematode parasites (GIN) is known be associated with life‐history traits and vital rates in wild vertebrate systems. To date, measurement of levels of antibodies against GIN antigens in natural populations has exclusively been based on invasive blood sampling techniques. Previous work in laboratory rodents and ruminant livestock suggests that antibody measures from feces may provide a viable noninvasive approach. We measured total and anti‐GIN antibodies of different isotypes (immunoglobulin (Ig) G, IgA and IgE) from paired samples of plasma and feces from free‐living Soay sheep of different ages and sexes. We tested the correlations among these measures as well as their associations with body mass and Strongyle nematode fecal egg counts (FEC). Significant positive correlations were present among plasma and fecal anti‐GIN antibody levels for IgG and IgA. Generally, correlations between total antibody levels in plasma and feces were weaker and not significant. No significant relationships were found between any antibody measures and body mass; however, fecal anti‐GIN antibody levels were significantly negatively correlated with FEC. Our data clearly demonstrate the feasibility of measuring anti‐GIN antibodies from fecal samples collected in natural populations. Although associations of fecal antibody levels with their plasma counterparts and FEC were relatively weak, the presence of significant correlations in the predicted direction in a relatively small and heterogeneous sample suggests fecal antibody measures could be a useful, noninvasive addition to current eco‐immunological studies.     

No correlation between multi‐locus heterozygosity and fitness in the common buzzard despite heterozygote advantage for plumage colour

Correlations between heterozygosity and fitness are frequently found but rarely well understood. Fitness can be affected by single loci of large effect which correlate with neutral markers via linkage disequilibrium, or as a result of variation in genome‐wide heterozygosity following inbreeding. We explored these alternatives in the common buzzard, a raptor species in which three colour morphs differ in their lifetime reproductive success. Using 18 polymorphic microsatellite loci, we evaluated potential genetic differences among the morphs which may lead to subpopulation structuring and tested for correlations between three fitness‐related traits and heterozygosity, both genome wide and at each locus separately. Despite their assortative mating pattern, the buzzard morphs were found to be genetically undifferentiated. Multilocus heterozygosity was only found to be correlated with a single fitness‐related trait, infection with the blood parasite, Leucocytozoon buteonis, and this was via interactions with vole abundance and age. One locus also showed a significant relationship with blood parasite infection and ectoparasite infestation. The vicinity of this locus contains two genes, one of which is potentially implicated in the immune system of birds. We conclude that genome‐wide heterozygosity is unlikely to be a major determinant of parasite burden and body condition in the polymorphic common buzzard.     

Genetic structure and host–parasite co‐divergence: evidence for trait‐specific local adaptation

Host–parasite co‐evolution can lead to genetic differentiation among isolated host–parasite populations and local adaptation between parasites and their hosts. However, tests of local adaptation rarely consider multiple fitness‐related traits although focus on a single component of fitness can be misleading. Here, we concomitantly examined genetic structure and co‐divergence patterns of the trematode Coitocaecum parvum and its crustacean host Paracalliope fluviatilis among isolated populations using the mitochondrial cytochrome oxidase I gene (COI). We then performed experimental cross‐infections between two genetically divergent host–parasite populations. Both hosts and parasites displayed genetic differentiation among populations, although genetic structure was less pronounced in the parasite. Data also supported a co‐divergence scenario between C. parvum and P. fluviatilis potentially related to local co‐adaptation. Results from cross‐infections indicated that some parasite lineages seemed to be locally adapted to their sympatric (home) hosts in which they achieved higher infection and survival rates than in allopatric (away) amphipods. However, local, intrinsic host and parasite characteristics (host behavioural or immunological resistance to infections, parasite infectivity or growth rate) also influenced patterns of host–parasite interactions. For example, overall host vulnerability to C. parvum varied between populations, regardless of parasite origin (local vs. foreign), potentially swamping apparent local co‐adaptation effects. Furthermore, local adaptation effects seemed trait specific; different components of parasite fitness (infection and survival rates, growth) responded differently to cross‐infections. Overall, data show that genetic differentiation is not inevitably coupled with local adaptation, and that the latter must be interpreted with caution in a multi‐trait context.     

PARASITE-MEDIATED SELECTION AGAINST INBRED SOAY SHEEP IN A FREE-LIVING ISLAND POPULATON

Parasites are thought to provide a selective force capable of promoting genetic variation in natural populations. One rarely considered pathway for this action is via parasite-mediated selection against inbreeding. If parasites impose a fitness cost on their host and the offspring of close relatives have greater susceptibility to parasites due to the increased homozygosity that results from inbreeding, then parasite-mediated mortality may select against inbred individuals. This hypothesis has not yet been tested within a natural vertebrate population. Here we show that relatively inbred Soay sheep (Ovis aries), as assessed by microsatellite heterozygosity, are more susceptible to parasitism by gastrointestinal nematodes, with interactions indicating greatest susceptibility among adult sheep at high population density. During periods of high overwinter mortality on the island of Hirta, St. Kilda, Scotland, highly parasitised individuals were less likely to survive. More inbred individuals were also less likely to survive, which is due to their increased susceptibility to parasitism, because survival was random with respect to inbreeding among sheep that were experimentally cleared of their gastrointestinal parasite burden by anthelminthic treatment. As a consequence of this selection, average microsatellite heterozygosity increases with age in St. Kildan Soay sheep. We suggest that parasite-mediated selection acts to maintain genetic variation in this small island population by removing less heterozygous individuals.     

Association between host's genetic diversity and parasite burden in damselflies

Recent research indicates that low genetic variation in individuals can increase susceptibility to parasite infection, yet evidence from natural invertebrate populations remains scarce. Here, we studied the relationship between genetic heterozygosity, measured as AFLP‐based inbreeding coefficient f_AFLP, and gregarine parasite burden from eleven damselfly, Calopteryx splendens, populations. We found that in the studied populations, 5–92% of males were parasitized by endoparasitic gregarines (Apicomplexa: Actinocephalidae). Number of parasites ranged from none to 47 parasites per male, and parasites were highly aggregated in a few hosts. Mean individual f_AFLP did not differ between populations. Moreover, we found a positive association between individual's inbreeding coefficient and parasite burden. In other words, the more homozygous the individual, the more parasites it harbours. Thus, parasites are likely to pose strong selection pressure against inbreeding and homozygosity. Our results support the heterozygosity‐fitness correlation hypothesis, which suggests the importance of heterozygosity for an individual's pathogen resistance.     

Sex differences in leucocyte telomere length in a free‐living mammal

Mounting evidence suggests that average telomere length reflects previous stress and predicts subsequent survival across vertebrate species. In humans, leucocyte telomere length (LTL) is consistently shorter during adulthood in males than in females, although the causes of this sex difference and its generality to other mammals remain unknown. Here, we measured LTL in a cross‐sectional sample of free‐living Soay sheep and found shorter telomeres in males than in females in later adulthood (>3 years of age), but not in early life. This observation was not related to sex differences in growth or parasite burden, but we did find evidence for reduced LTL associated with increased horn growth in early life in males. Variation in LTL was independent of variation in the proportions of different leucocyte cell types, which are known to differ in telomere length. Our results provide the first evidence of sex differences in LTL from a wild mammal, but longitudinal studies are now required to determine whether telomere attrition rates or selective disappearance are responsible for these observed differences.     

Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

Climate change is expected to alter the dynamics of host–parasite systems globally. One key element in developing predictive models for these impacts is the life cycle of the parasite. It is, for example, commonly assumed that parasites with an indirect life cycle would be more sensitive to changing environmental conditions than parasites with a direct life cycle due to the greater chance that at least one of their obligate host species will go extinct. Here, we challenge this notion by contrasting parasitic nematodes with a direct life cycle against those with an indirect life cycle. Specifically, we suggest that behavioral thermoregulation by the intermediate host may buffer the larvae of indirectly transmitted parasites against temperature extremes, and hence climate warming. We term this the ‘shelter effect’. Formalizing each life cycle in a comprehensive model reveals a fitness advantage for the direct life cycle over the indirect life cycle at low temperatures, but the shelter effect reverses this advantage at high temperatures. When examined for seasonal environments, the models suggest that climate warming may in some regions create a temporal niche in mid‐summer that excludes parasites with a direct life cycle, but allows parasites with an indirect life cycle to persist. These patterns are amplified if parasite larvae are able to manipulate their intermediate host to increase ingestion probability by definite hosts. Furthermore, our results suggest that exploiting the benefits of host sheltering may have aided the evolution of indirect life cycles. Our modeling framework utilizes the Metabolic Theory of Ecology to synthesize the complexities of host behavioral thermoregulation and its impacts on various temperature‐dependent parasite life history components in a single measure of fitness, R₀. It allows quantitative predictions of climate change impacts, and is easily generalized to many host–parasite systems.     

Lower survival probability of house sparrows severely infected by the gapeworm parasite

The effect of parasites in natural populations has received increasing attention in recent years. Studies have shown that parasites may play an important part in population ecology due to their potential effects on host fitness. The main purpose of the present study was to investigate the effect of a nematode parasite (gapeworm, Syngamus trachea) on survival probability of house sparrows Passer domesticus from six natural populations located on 4 islands in the Helgeland archipelago in northern Norway. Infection status was obtained from feces samples collected from 603 house sparrows in the summer and autumn of 2007–2011. We also collected data on a visible symptom of severe infection (gasping for air) in 1391 house sparrows in the summer and autumn 2004–2011. We took advantage of recent advances in disease modeling in a multi‐event capture–mark–recapture framework to account for imperfect observations (state uncertainty). Each dataset was separately analyzed, in both analyses we investigated the relationships of year, island, individual body condition, age class and population density with survival probabilities. The relationship between infection (determined by feces egg counts) on annual survival of house sparrows was not statistically significant. However, the probability of annual survival was found to be significantly lower for adult house sparrows exhibiting a symptom of severe gapeworm infection, gasping for air. The present study demonstrates that severe infection by a parasite can have a negative relationship with survival probability of short‐lived avian hosts in wild populations.     

Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load

There are substantial individual differences in parasite composition and infection load in wildlife populations. Few studies have investigated the factors shaping this heterogeneity in large wild mammals or the impact of parasite infections on Darwinian fitness, particularly in juveniles. A host's parasite composition and infection load can be shaped by factors that determine contact with infective parasite stages and those that determine the host's resistance to infection, such as abiotic and social environmental factors, and age. Host–parasite interactions and synergies between coinfecting parasites may also be important. We test predictions derived from these different processes to investigate factors shaping infection loads (fecal egg/oocyte load) of two energetically costly gastrointestinal parasites: the hookworm Ancylostoma and the intracellular Cystoisospora, in juvenile spotted hyenas (Crocuta crocuta) in the Serengeti National Park, in Tanzania. We also assess whether parasite infections curtail survival to adulthood and longevity. Ancylostoma and Cystoisospora infection loads declined as the number of adult clan members increased, a result consistent with an encounter‐reduction effect whereby adults reduced encounters between juveniles and infective larvae, but were not affected by the number of juveniles in a clan. Infection loads decreased with age, possibly because active immune responses to infection improved with age. Differences in parasite load between clans possibly indicate variation in abiotic environmental factors between clan den sites. The survival of juveniles (<365 days old) to adulthood decreased with Ancylostoma load, increased with age, and was modulated by maternal social status. High‐ranking individuals with low Ancylostoma loads had a higher survivorship during the first 4 years of life than high‐ranking individuals with high Ancylostoma loads. These findings suggest that high infection loads with energetically costly parasites such as hookworms during early life can have negative fitness consequences.